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Epigenetics in Plant Tissue Culture

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Epigenetics in Plant Tissue Culture Plant Growth Regul (2011) 63:137–146 DOI 10.1007/s10725-010-9531-4 SI : TISSUE CULTURE Epigenetics in plant tissue culture M. J. M. Smulders • G. J. de Klerk Received: 28 April 2010 / Accepted: 20 September 2010 / Published online: 8 October 2010 Ó The Author(s) 2010. This article is published with open access at Springerlink.com Abstract Plants produced vegetatively in tissue culture Klerk 2009). Researchers expected initially that these may differ from the plants from which they have been clonally propagated plants would be exact copies of the derived. Two major classes of off-types occur: genetic ones parent plant, but frequently aberrant plants were observed. and epigenetic ones. This review is about epigenetic aber- Various causes have been established: rations. We discuss recent studies that have uncovered • Genetic changes (also referred to as somaclonal vari- epigenetic modifications at the molecular level, viz., ation): changes in the DNA sequence; changes in DNA methylation and alterations of histone • Epigenetic variation: long-lasting changes in the methylation or acetylation. Various studies have been car- expression of the information in the genome; ried out with animals, and with plant cells or tissues that have • And—less relevant for this review—chimeral segrega- grown in tissue culture but only little work has been done tion and loss of pathogens, in particular viruses. with shoots generated by axillary branching. We present various molecular methods that are being used to measure Various types of genetic changes have been observed epigenetic variation. In micropropagated plants mostly dif- including polyploidy, aneuploidy, (point) mutations, and ferences in DNA methylation have been examined. Epige- new insertions of (retro) transposons. In crosses, mutations netic changes are thought to underlie various well-known behave as Mendelian traits, with the notable exception of tissue-culture phenomena including rejuvenation, habitua- plants that become ‘normal’ when an inserted transposon tion, and morphological changes such as flower abnormali- jumps out again. Epigenetic changes are caused by changes ties, bushiness, and tumorous outgrowths in, among others, in the expression of the information in the DNA brought oil palm, gerbera, Zantedeschia and rhododendron. about by alterations in DNA methylation, in histones, or in both. These modifications may influence gene transcrip- Keywords Methylation Á Micropropagation Á Off-types Á tion. Epigenetic changes are often temporary and plants Rejuvenation Á Habituation may revert to the normal phenotype relatively easily, but some can be long lasting and may even be transferred during sexual propagation (Brettell and Dennis 1991) Introduction (Fig. 1). The latter occurs regularly in plants as epigenetic marks are not systematically erased in embryogenesis, as In tissue culture, new plants may be generated by out- they are in mammals, and this leads to inheritable epimu- growth of axillary buds or by adventitious regeneration (De tations (epialleles) (Jullien and Berger 2010). Johannes et al. (2009) detected epigenetic changes in Arabidopsis This paper is dedicated to Dr. A. F. (Ton) Croes (1935–2009), friend, thaliana that were stable for at least eight generations. teacher and reference point. It is characteristic for epigenetic changes that in a population of generated plants the same aberration occurs & M. J. M. Smulders ( ) Á G. J. de Klerk at high frequency and can be ‘reproduced’ when the same Wageningen UR Plant Breeding, P.O. Box 16, 6700 AA Wageningen, The Netherlands conditions are imposed during the production of another e-mail: [email protected] population (Smulders et al. 1995). In contrast, genetic 123 138 Plant Growth Regul (2011) 63:137–146 Fig. 1 Schematic representation of the differences between genetic and epigenetic variation. Note that during the various indicated tissue culture processes, the extent of genetic variation remains the same, but the extent of epigenetic variation is sharply reduced. In plants some epigenetic changes may survive sexual propagation changes occur at random. It should be noted that in a (Tessadori et al. 2007). On the other hand, epigenetic somaclonal population the same genetic change may be mechanisms regulate gene expression during development: found in many individuals but then the mutational event genes may be methylated and switched off in some tissues, happened early during the tissue culture period and was but demethylated and active in others (see Matzke et al. clonally multiplied into a number of descendants (Brettell 2009 for a description of the mechanism and the genes and Dennis 1991; Kohli et al. 2004). involved). The clearest examples of this type of epigenetic regulation are found in mammalian embryogenesis: imprinting (where the activity of a gene in early embryo Characteristics of epigenetic changes development depends on whether it is inherited from the father or the mother), X-inactivation (to achieve the proper Epigenetic mechanisms include DNA methylation and gene dosage, one of the two X chromosomes in females is modifications of amino acids in the tails of histones. His- heavily methylated and transcription is largely switched tones are proteins that package the DNA into nucleosomes off), and reprogramming (of genome-wide DNA methyla- and make up the chromatin in nuclei. DNA methylation tion patterns in the gastrula stage). Imprinting also occurs and histone modifications interact and reinforce one during plant endosperm development (Hsieh et al. 2009). another. In this way, transcription can be enhanced, for When ‘genes’ are said to be methylated and transcrip- example, by acetylation of the lysine on position 9 of tionally silenced, it is actually the promotor region that histone 3 (‘H3K9’), which is found in promotor regions of becomes methylated, as even actively transcribed genes actively transcribed genes. Transcription can also be may be methylated in the ‘body’ of the coding region, i.e., decreased, for example, by di- and trimethylation of H3K9, at some distance from the 50 and 30 end (Roudier et al. which is a histone mark of repeat elements in the DNA 2009; Tanurdzic et al. 2008). (Bernatavichute et al. 2008; Tessadori et al. 2007). Repeat During plant development, the epigenetic imprints pro- elements are also characterized by methylation of cytosines vide a transient ‘memory’ of the developmental program in the DNA. and influence the cell’s reactions and its future develop- This regulatory system has several functions. On the one ment (Roudier et al. 2009). A notable example of the hand, it is a defence mechanism against retrotransposons. memory function is vernalization, the acquisition or Silencing of repeats is thought to occur in all cells, acceleration of the ability to flower by a chilling treatment. regardless of their location or developmental state. It is In Arabidopsis, vernalization involves the silencing of a targeted by 21- and 24-mer short RNAs. Intriguingly, the group of flowering repressor genes, including Flowering same mechanism contributes to sustain the centromere Locus C (FLC; Bastow et al. 2004; Roudier et al. 2009). through silencing and compacting the centromeric repeats Silencing occurs during a cold period through an epigenetic 123 Plant Growth Regul (2011) 63:137–146 139 change, viz., through histone modifications (Bastow et al. correlate with particular morphological or physiological 2004; Kim et al. 2009). Interestingly, in barley it is med- abnormalities observed in regenerants (Jaligot et al. 2002; iated by different histone modifications at the floral acti- Smulders et al. 1995). Possible correlations between the vator gene VERNALIZATION1 (VRN1), allowing it to amount of changes at the molecular level and the extent of become active (Oliver et al. 2009) Another example is the abnormalities may be established by studying many more phase change from juvenile to adult, which is paralleled by sites. Technically, such research is becoming possible. changes in gross DNA methylation (Valledor et al. 2007). However, if specific stretches of DNA, e.g., in a particular De Klerk (1990) and Va´zquez (2001), amongst others, promotor, affect the expression of a specific gene that leads noted that the distinction between genetic and epigenetic to one type of change, an estimation of the overall level of changes is an oversimplification. Molecular evidence has variation would not necessarily provide a strong correlation accumulated showing that epigenetic changes may lead to with the specific abnormality under study. many genetic abnormalities. The transposable element It may be easier to study changes that occur repeatedly Activator (Ac) in maize looses DNA methylation and as the correlation of certain changes in DNA and histone becomes activated upon dedifferentiation (Brettell and modifications with the phenotypic changes can be deter- Dennis 1991). The same occurs in transgenic rice plants mined and used as a selection criterion. In cancer research, containing Ac from maize (Kohli et al. 2004). In maize, the this yields interesting results (certain aberrantly methylated activation is passed on for two sexual generations (Brettell CpG islands in the genome are biomarkers for several types and Dennis 1991). The miniature inverted repeat trans- of cancer). The progression of a cancer goes through sev- posable element (MITE) mPing becomes activated in rice, eral specific stages, including an initial step of massive e.g., in callus culture, which is correlated with alterations
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